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PMID: 8041748 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cell-surface receptors for gibbon ape leukemia virus and amphotropic murine retrovirus are inducible sodium-dependent phosphate symporters.

Kavanaugh MP, Miller DG, Zhang W, Law W, Kozak SL, Kabat D, Miller AD

Abstract

Cell surface receptors for gibbon ape leukemia virus (Glvr-1) and murine amphotropic retrovirus (Ram-1) are distinct but related proteins having multiple membrane-spanning regions. Distant homology with a putative phosphate permease of Neurospora crassa suggested that these receptors might serve transport functions. By expression in Xenopus laevis oocytes and in mammalian cells, we have identified Glvr-1 and Ram-1 as sodium-dependent phosphate symporters. Two-electrode voltage-clamp analysis indicates net cation influx, suggesting that phosphate is transported with excess sodium ions. Phosphate uptake was reduced by > 50% in mouse fibroblasts expressing amphotropic envelope glycoprotein, which binds to Ram-1, indicating that Ram-1 is a major phosphate transporter in these cells. RNA analysis shows wide but distinct tissue distributions, with Glvr-1 expression being highest in bone marrow and Ram-1 in heart. Overexpression of Ram-1 severely repressed Glvr-1 synthesis in fibroblasts, suggesting that transporter expression may be controlled by net phosphate accumulation. Accordingly, depletion of extracellular phosphate increased Ram-1 and Glvr-1 expression 3- to 5-fold. These results suggest simple methods to modulate retroviral receptor expression, with possible applications to human gene therapy.

MeSH Terms
3T3 Cells Animals Biological Transport Carrier Proteins/metabolism Cell Line Gene Expression Humans Leukemia Virus, Gibbon Ape/metabolism Leukemia Virus, Murine/metabolism Mice Oocytes Phosphate Transport Proteins Phosphate-Binding Proteins Phosphates/metabolism Rats Receptors, Virus/genetics,metabolism Recombinant Proteins Sodium/metabolism Sodium-Phosphate Cotransporter Proteins Sodium-Phosphate Cotransporter Proteins, Type III Symporters Xenopus laevis
Chemicals
Carrier Proteins Phosphate Transport Proteins Phosphate-Binding Proteins Phosphates Receptors, Virus Recombinant Proteins SLC20A1 protein, human Slc20a1 protein, mouse Slc20a1 protein, rat Slc20a2 protein, mouse Slc20a2 protein, rat Sodium-Phosphate Cotransporter Proteins Sodium-Phosphate Cotransporter Proteins, Type III Symporters leukemia virus receptor, gibbon ape Sodium
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Kavanaugh M P
Vollum Institute for Advanced Biomedical Research, Oregon Health Sciences University, Portland 97201.
Miller D G
Zhang W
Law W
Kozak S L
Kabat D
Miller A D
References (45)
45 references, click to expand
  1. Production of human factor IX in animals by genetically modified skin fibroblasts: potential therapy for hemophilia B.
    Blood. 1989 Feb;73(2):438-45 PMID: 2917183
  2. Cloning of a Na/Pi cotransporter from opossum kidney cells.
    J Biol Chem. 1994 Mar 4;269(9):6615-21 PMID: 7509808
  3. Depletion of the surface CD4 molecule by the envelope protein of human immunodeficiency virus expressed in a human CD4+ monocytoid cell line.
    J Virol. 1989 Sep;63(9):3748-54 PMID: 2788223
  4. Nucleotide sequence of pho-4+, encoding a phosphate-repressible phosphate permease of Neurospora crassa.
    Gene. 1989 Nov 30;83(2):281-9 PMID: 2531109
  5. Phosphate transport processes in eukaryotic cells.
    J Membr Biol. 1989 Nov;111(3):199-213 PMID: 2557449
  6. Sodium-phosphate cotransport in OK cells: inhibition by PTH and "adaptation" to low phosphate.
    Am J Physiol. 1989 Dec;257(6 Pt 2):F967-73 PMID: 2557766
  7. Molecular cloning and characterization of a defective recombinant feline leukaemia virus associated with myeloid leukaemia.
    J Gen Virol. 1990 Feb;71 ( Pt 2):343-54 PMID: 2155287
  8. CD4: collaborator in immune recognition and HIV infection.
    Cell. 1990 Mar 9;60(5):697-700 PMID: 2107022
  9. Improved retroviral vectors for gene transfer and expression.
    Biotechniques. 1989 Oct;7(9):980-2, 984-6, 989-90 PMID: 2631796
  10. From cell membrane to nucleotides: the phosphate regulon in Escherichia coli.
    Bioessays. 1990 Aug;12(8):371-6 PMID: 2241934
  11. Characterization of a human gene conferring sensitivity to infection by gibbon ape leukemia virus.
    Cell Growth Differ. 1990 Mar;1(3):119-27 PMID: 2078500
  12. Serine phosphorylation-independent downregulation of cell-surface CD4 by nef.
    Nature. 1991 Apr 11;350(6318):508-11 PMID: 2014052
  13. Construction and properties of retrovirus packaging cells based on gibbon ape leukemia virus.
    J Virol. 1991 May;65(5):2220-4 PMID: 1850008
  14. Infectious primate type C viruses: Three isolates belonging to a new subgroup from the brains of normal gibbons.
    Virology. 1975 Oct;67(2):335-43 PMID: 52939
  15. Transformation of mammalian cells by avian myelocytomatosis virus and avian erythroblastosis virus.
    Virology. 1979 Oct 30;98(2):461-5 PMID: 228482
  16. Oncogenicity of gibbon type-C myelogenous leukemia virus.
    Int J Cancer. 1980 May 15;25(5):641-6 PMID: 6768682
  17. Some factors affecting phosphate transport in a perfused rat heart preparation.
    Biochem J. 1980 May 15;188(2):297-11 PMID: 7396864
  18. Construction and isolation of a transmissible retrovirus containing the src gene of Harvey murine sarcoma virus and the thymidine kinase gene of herpes simplex virus type 1.
    J Virol. 1981 Sep;39(3):935-44 PMID: 6270359
  19. Two base changes restore infectivity to a noninfectious molecular clone of Moloney murine leukemia virus (pMLV-1).
    J Virol. 1984 Jan;49(1):214-22 PMID: 6197537
  20. A method for isolation of intact, translationally active ribonucleic acid.
    DNA. 1983;2(4):329-35 PMID: 6198133
  21. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain.
    Cell. 1986 Nov 7;47(3):333-48 PMID: 3094962
  22. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production.
    Mol Cell Biol. 1986 Aug;6(8):2895-902 PMID: 3785217
  23. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  24. Transduction of endogenous envelope genes by feline leukaemia virus in vitro.
    Nature. 1988 Apr 21;332(6166):731-4 PMID: 2895894
  25. The PHO84 gene of Saccharomyces cerevisiae encodes an inorganic phosphate transporter.
    Mol Cell Biol. 1991 Jun;11(6):3229-38 PMID: 2038328
  26. Transport of cationic amino acids by the mouse ecotropic retrovirus receptor.
    Nature. 1991 Aug 22;352(6337):725-8 PMID: 1652100
  27. Cell-surface receptor for ecotropic murine retroviruses is a basic amino-acid transporter.
    Nature. 1991 Aug 22;352(6337):729-31 PMID: 1908564
  28. Plasma membrane receptors for ecotropic murine retroviruses require a limiting accessory factor.
    J Virol. 1991 Dec;65(12):6468-77 PMID: 1942243
  29. Cloning and expression of cDNA for a Na/Pi cotransport system of kidney cortex.
    Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9608-12 PMID: 1946375
  30. Retroviral pseudotypes produced by rescue of a Moloney murine leukemia virus vector by C-type, but not D-type, retroviruses.
    Virology. 1992 Feb;186(2):792-4 PMID: 1733113
  31. GLVR1, a receptor for gibbon ape leukemia virus, is homologous to a phosphate permease of Neurospora crassa and is expressed at high levels in the brain and thymus.
    J Virol. 1992 Mar;66(3):1635-40 PMID: 1531369
  32. Electrogenic uptake of gamma-aminobutyric acid by a cloned transporter expressed in Xenopus oocytes.
    J Biol Chem. 1992 Nov 5;267(31):22007-9 PMID: 1429551
  33. Effects of ecotropic murine retroviruses on the dual-function cell surface receptor/basic amino acid transporter.
    J Biol Chem. 1992 Nov 25;267(33):23617-24 PMID: 1429703
  34. Human immunodeficiency virus type 1 Vpu protein induces rapid degradation of CD4.
    J Virol. 1992 Dec;66(12):7193-200 PMID: 1433512
  35. Isolation and characterization of a 2.3-kilobase-pair cDNA fragment encoding the binding domain of the bovine leukemia virus cell receptor.
    J Virol. 1993 Feb;67(2):1050-7 PMID: 8380453
  36. Cloning and expression of a mammalian Na+/amino acid cotransporter with sequence similarity to Na+/glucose cotransporters.
    J Biol Chem. 1993 Jan 25;268(3):1509-12 PMID: 8420925
  37. Recombinant feline leukemia virus genes detected in naturally occurring feline lymphosarcomas.
    J Virol. 1993 Jun;67(6):3118-25 PMID: 8388492
  38. Expression cloning of human and rat renal cortex Na/Pi cotransport.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):5979-83 PMID: 8327470
  39. Retrovirus-mediated gene transfer into rhesus monkey hematopoietic stem cells: the effect of viral titers on transduction efficiency.
    Hum Gene Ther. 1993 Jun;4(3):239-47 PMID: 8338872
  40. Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family.
    J Biol Chem. 1993 Jul 25;268(21):15329-32 PMID: 8101838
  41. A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor.
    Cell. 1993 Sep 24;74(6):1043-51 PMID: 8402880
  42. Definition of a domain of GLVR1 which is necessary for infection by gibbon ape leukemia virus and which is highly polymorphic between species.
    J Virol. 1993 Nov;67(11):6733-6 PMID: 8411375
  43. Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus.
    Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):78-82 PMID: 8278411
  44. A human amphotropic retrovirus receptor is a second member of the gibbon ape leukemia virus receptor family.
    Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1168-72 PMID: 8302848
  45. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection.
    Cell. 1989 May 19;57(4):659-66 PMID: 2541919
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1994-07-19
Pages
7071-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC44340
Subset
IM
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